Impaired Speaking-Induced Suppression in Alzheimer's Disease

Abstract

Alzheimer's disease (AD) is a neurodegenerative disease involving cognitive impairment and abnormalities in speech and language. Here, we examine how AD affects the fidelity of auditory feedback predictions during speaking. We focus on the phenomenon of speaking-induced suppression (SIS), the auditory cortical responses' suppression during auditory feedback processing. SIS is determined by subtracting the magnitude of auditory cortical responses during speaking from listening to playback of the same speech. Our state feedback control (SFC) model of speech motor control explains SIS as arising from the onset of auditory feedback matching a prediction of that feedback onset during speaking, a prediction that is absent during passive listening to playback of the auditory feedback. Our model hypothesizes that the auditory cortical response to auditory feedback reflects the mismatch with the prediction: small during speaking, large during listening, with the difference being SIS. Normally, during speaking, auditory feedback matches its predictions, then SIS will be large. Any reductions in SIS will indicate inaccuracy in auditory feedback prediction not matching the actual feedback. We investigated SIS in AD patients [n = 20; mean (SD) age, 60.77 (10.04); female (%), 55.00] and healthy controls [n = 12; mean (SD) age, 63.68 (6.07); female (%), 83.33] through magnetoencephalography (MEG)-based functional imaging. We found a significant reduction in SIS at ∼100 ms in AD patients compared with healthy controls (linear mixed effects model, F _(1,57.5) = 6.849, p = 0.011). The results suggest that AD patients generate inaccurate auditory feedback predictions, contributing to abnormalities in AD speech.

Keywords: Alzheimer’s disease; efference copy; magnetoencephalography; speaking-induced suppression; state feedback control model.

Figure 1.

Auditory cortical time course in both the speaking and listening conditions. MEG traces were aligned to the voice onset. Thick lines denote means, and the shaded regions behind the lines denote SEM (blue, the listening condition; red, the speaking condition). A, B, AD patients’ mean responses (n = 20) for the left hemisphere (A) and the right hemisphere (B) are depicted. C, D, The mean responses for healthy controls (HC; n = 12) are shown in the left hemisphere (C) and the right hemisphere (D).

Figure 2.

Amplitudes at M50, M100, and M200 in auditory cortical time course. AD patients’ data (AD; n = 20; mean ± SEM) are presented in gray. Healthy controls’ data (HC; n = 12; mean ± SEM) are in white. A, B, The means of individual SIS magnitudes at each peak are exhibited in the left (A) and right (B) hemispheres. C, D, The means of amplitudes at the three peaks from the cortical activity during speaking are depicted in the left (C) and right (D) hemispheres. E, F, The mean peak values of cortical responses during listening are displayed in the left (E) and right (F) hemispheres.

Figure 3.

Latencies at M50, M100, and M200 in auditory cortical time course. AD patients’ data (AD; n = 20; mean ± SEM) and healthy controls’ data (HC; n = 12; mean ± SEM) are gray and white, respectively. A, C, E, In the left hemisphere, the average latencies are depicted in the speaking condition (C), the listening condition (E), and the latency difference between the two conditions (A). B, D, F, In the right hemisphere, the average latencies are shown in the speaking condition (D), the listening condition (F), and the latency difference between the two conditions (B).